Dichelobacter nodosus infection
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Dichelobacter nodosus infection
International Common Names
- English: benign foot rot; bumblefoot; contagious foot rot; foot abscess; foot rot; foot scald; footrot; heel abscess; infectious pododermatitis; infective bulbar necrosis; interdigital infection in goats, foot rot, footrot; interdigital necrobacillosis; malignant foot rot; ovine contagious footrot, foot rot, scald, foot abscess; ovine interdigital dermatitis; piétin; pododermatitis; scald; underrun heels, erosion of the hoof, heel cracks in ruminants and pigs; virulent foot rot
- Spanish: piepodrido
Local Common Names
- Germany: moderhinke
- Italy: zoppina
- Netherlands: rotkreupel
OverviewTop of page
Lameness in ruminants affects productivity and impairs animal welfare worldwide. In temperate regions and at higher altitudes in sub-tropical regions, a lot of the lameness observed is associated with infection by Dichelobacter nodosus. This bacterium, originally described as Fusiformis nodosus, was first isolated from cases of footrot in sheep in Australia (Beveridge, 1941). Subsequently the organism was isolated and described in cattle, goats deer and mouflon, in diseases analogous to ovine footrot (Egerton, 1989; Nattermann et al., 1990). Although previously considered to belong to the family Bacteroidaceae, the correct taxonomic position of the footrot organism was resolved by Dewhirst et al. (1990) who placed it in a distinct genus of the family Cardiobacteriaceae.
While D. nodosus is the transmitting agent of footrot, it always occurs in association with other potential and perhaps contributory pathogens. Of these, Fusobacterium necrophorum and species of Spirochaeta have been have been attributed roles in the disease (Beveridge, 1941, Roberts and Egerton,1969). More recently a severe disease of sheep`s feet associated with spirochaetes in the absence of D. nodosus, has been described (Naylor et al., 1998; Davies et al., 1999). However, because it is the transmitting agent of footrot, D. nodosus has been the focus of research and the basis of management systems for ovine footrot.
Ovine footrot was recognized as a contagious disease for many years before D. nodosus was identified. It has a major impact on the profitability of sheep grazing in Europe, Australia, New Zealand, Argentina, Brazil, Uruguay and in some states of the USA. Disease manifestation can range from low to high prevalence depending on host, bacterial, environmental and climatic conditions, resulting in benign, intermediate and virulent forms of footrot. Methods for the control of ovine footrot include eradication of non-benign disease from affected flocks, control largely through vaccination, topical and systemic treatment and preventative measures through strategic vaccination (reviewed by Raadsma and Egerton, 2013).
Bovine infections with D. nodosus may be sub-clinical, cause lameness or result in serious sequelae. (Toussaint and Cornelisse, 1971; Thorley and Calder, 1977; Laing and Egerton, 1978; Egerton, 1989).
Hosts/Species AffectedTop of page
The role of different ruminant species as alternate hosts is discussed in the epidemiology text. The common factor that predisposes animals to infection by D. nodosus is chronic exposure of the interdigital skin to water and faeces. In some countries this occurs regularly with grazing at pasture. The nature of the pasture may affect the prevalence of the disease observed. Improved pastures with a high clover component favour the disease (Beveridge, 1941). The nature of the sward influences the capacity of the undercover to retain water, and hence maintain the hydration and devitalization of the cornified layer of the interdigital skin. Where animals are kept indoors for long periods, for example dairy cattle in Europe and North America, they are constantly exposed to conditions that predispose to infection by D. nodosus if it is present. Where sheep are housed in winter the physical environment is suitable for transmission of footrot. It is important to reaffirm that exposure to water and the organisms in ruminant faeces are alone insufficient to cause footrot. D. nodosus must be present in the environment.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Bhutan||Present||Kelly, 1990; Gurung et al., 2006|
|China||Present||Wang et al., 1999|
|India||Present||Present based on regional distribution.|
|-Jammu and Kashmir||Present||Taku et al., 2010|
|Iraq||Present||Rhaymah et al., 1993|
|Malaysia||Present||Present based on regional distribution.|
|-Peninsular Malaysia||Present||Zunita et al., 1998|
|Nepal||Present||Ghimire et al., 1997|
|Comoros||Present||John et al., 1990|
|South Africa||Localised||Bath, 2000|
|Canada||Present||Olson et al., 1998|
|-Alberta||Present||Olson et al., 1998|
|-British Columbia||Present||Olson et al., 1998|
|USA||Widespread||Gradin et al., 1993|
|-California||Present||Lee et al., 1993|
|-Oregon||Present||Lee et al., 1993|
|-West Virginia||Present||Lee et al., 1993|
|Brazil||Ribeiro, 1994; Silva et al., 1999|
|Uruguay||Present||Hirigoyen and Bermudez, 1991|
|Austria||Present||Friedrich et al., 2012|
|Germany||Present||Younan et al., 1999; Friedrich et al., 2012|
|Italy||Present||Pedrona et al., 1989|
|Netherlands||Present||Toussaint and Cornelisse, 1971|
|Norway||Present||Rogdo et al., 2012|
|Poland||Present||Cygan and Buczek, 1995|
|Romania||Present||Moldovan et al., 1986|
|Russian Federation||Present||Present based on regional distribution.|
|-Russia (Europe)||Present||Semenova et al., 1988|
|Spain||Present||Hurtado et al., 1998|
|Sweden||Present||König et al., 2011|
|Switzerland||Present||Friedrich et al., 2012; Härdi-Landerer et al., 2012|
|UK||Widespread||Roberts and Walker, 1973; Walker et al., 1973; Thorley, 1976; Thorley and Calder, 1977; Hindmarsh et al., 1989; Green and George, 2008|
|Yugoslavia (former)||Present||Hristov et al., 1998|
|Australia||Present||Present based on regional distribution.|
|-New South Wales||Widespread||Walker, 1997|
|-South Australia||Localised||McFarland and Saunders, 1996|
|-Tasmania||Widespread||McFarland and Saunders, 1996|
|-Victoria||Widespread||Rendell and Callinan, 1997|
|-Western Australia||Localised||Depiazzi and Richards, 1979|
|New Zealand||Present||Liardet et al., 1989|
PathologyTop of page
Infection with D. nodosus results in the development of an acute epidermitis. This leads to the disruption of keratinization, either in the interdigital skin or in the horn of the hoof, or in both. Therefore the predominant macroscopic lesion in virulent footrot is abnormal, distorted cornified tissue. When the disease is chronic, gross overgrowth of the affected horn may be obvious. Infection with mixed bacteria, which occurs in footrot, results in the migration of many monocytic and neutrophilic leucocytes to the epidermis. This infiltration originates in the capillaries of that part of the dermis that is opposing the affected area of the epidermis. The bacterial invasion does not extend beyond the germinal layer of the epidermis. The invasion and inflammation is accompanied by serous exudate, and hydropic degeneration and necrosis of affected cells (Stewart, 1989).
DiagnosisTop of page
It is important to distinguish between the diagnosis of individual cases of footrot and assessing the clinical form of the disease present in a flock. The latter decision will determine whether or not intervention at the flock level is justified (Egerton and Raadsma, 2000)
Diagnosis of cases of ovine footrot
The principal clinical sign is lameness, although all affected animals may not be lame. Animals with severe disease are lighter and have tender wool. They are often recumbent and may develop pressure ulcers on the sternum. Examination of the feet will reveal the presence of some or all of the following signs:
- An inflamed interdigital skin(IDS).
- An IDS surface that is covered with a film of serous exudate and necrotic epidermal tissue.
- An over-grown and distorted hoof horn, which is separated from its underlying tissue to a greater or lesser degree.
All four feet may be affected, but only one digit of one foot may be involved. The odour of affected feet is characteristic.
Other causes of lameness need to be considered and eliminated. These include foot and mouth disease (FMD), blue tongue disease (BTD) and metabolic or non-suppurative laminitis. History of access to feed concentrates and the absence of signs of necrotic tissue will assist in diagnozing the latter. The primary lesions in FMD are vesicles in either the mouth and/or feet, and if seen early do not resemble those of footrot. However, in areas where both diseases are endemic, differential diagnosis of more chronic cases may be more difficult. It is possible for new cases of FMD to occur in animals where footrot is already present. The feature common to blue tongue disease and footrot is lameness. In the former, there may be an acute coronitis, but again there is an absence of necrosis of the tissues of the hoof and there will be signs of BTD in other tissues.
Other diseases that often occur in the same environments as footrot are foot abscess, lamellar suppuration, ovine interdigital dermatitis, post-dipping lameness and contagious pustular dermatitis (CPD). The lameness of foot abscess is more severe than that seen in footrot, the affected foot is usually swollen and held from the ground. Characteristically, there is copious discharge of necrotic material from sinuses, either in the interdigital cleft or above the coronary band. Stained smears of sinus discharge show numerous leucocytes and filaments of F. necrophorum.
Lamellar suppuration or toe abscess also causes acute lameness, usually in one of the fore feet. It results from the localization of environmental bacteria in sensitive laminae that have been exposed mechanically, or through the fracture of overgrown horns at the toe region of sheep grazing continually on wet pasture. Only sporadic cases occur and multiple affected feet in the one sheep are rare.
Ovine interdigital dermatitis (OID) is a mild disease of the interdigital skin of sheep chronically exposed to wet, faecally contaminated environments. The inflammation and occasional lameness results from a superficial invasion of the epidermis by F. necrophorum and Actinomyces pyogenes (Egerton et al., 1969). OID occurs in the absence of D. nodosus and disappears as the environment dries.
Post dipping lameness is a specific form of lamellar suppuration. It causes a high prevalence of lameness within 7 days of sheep being dipped in fluids contaminated with Erysipelothrix insidiosa (Watkins, 2000).
CPD normally occurs in the buccal area of affected animals. In some animals, lesions occur only in the interdigital skin, and when secondarily infected this results in a dermatitis superficially resembling the early stages of footrot. The presence of typical mouth lesions in some members of the flock will assist diagnosis.
Microscopy: Careful examination of a stained smear of a thin film of necrotic material from a case of footrot will reveal the characteristic, terminally swollen, Gram negative rods of D. nodosus. The organism may also be detected specifically with fluorescein labelled antibody (Roberts and Walker, 1973). Often they are the least frequent of the bacteria in such smears. This is especially so when they are taken from a chronically under-run horn. Better results are obtained from smears taken from affected interdigital skin, not grossly contaminated with mud or faecal material. A positive smear confirms the presence of footrot, but does not indicate the clinical form of the disease affecting either the individual or the flock.
Isolation and characterization: With the correct techniques and appropriate medium
(Skerman, 1989), it is possible to isolate D. nodosus from 70% or more of clinical samples. Primary isolation is enhanced by the use of 4% agar in plates of enriched medium (Thorley, 1976). This concentration inhibits spreading organisms, which otherwise over-run cultures during the 3-4 days needed for the growth of D. nodosus. This concentration of agar also enhances the twitching mobility of the organism and colonies spread in a characteristic flat, etched glass fashion beyond the streaks of inoculum. The inoculum is usually contaminated with many other species. Sub-cultures taken from the edge of the D. nodosus colonies are transferred to fresh 4% agar plates. When free of contaminants colonies are sub-cultured to 2% agar.
A number of tests are available for demonstrating and characterizing enzymes elaborated by D. nodosus in vitro. The elastase test (Skerman, 1977; Stewart, 1979) differentiates virulent and benign isolates of the organism. The more virulent isolates digest elastin within 5-10 days incubation, whereas benign strains take more than 18 days. The thermostability of the organisms’ proteases have also been used to differentiate virulent from benign isolates (Depiazzi and Richards, 1979; Palmer, 1993). Electrophoretic analysis of proteases (the Zymogram test) also allows discrimination between isolates of different virulence (Every, 1982; Kortt et al., 1983). The qualitative differences between proteases have been exploited in a protease ELISA test (Links et al., 1995). While all these tests have been shown to discriminate between different categories of isolates in vitro, their ability to determine the severity of outbreaks of disease is less certain. Whittington (1994) identified some of the arguments against the adoption of protease based tests for the classification of disease outbreaks.
- There is no general agreement for a gold standard determination of virulence as applied to different clinical manifestations of footrot at the flock level.
- It is known that most outbreaks are associated with multiple strains of the organism (Claxton et al, 1983; Zhou and Hickford, 2000) and there are unresolved sampling problems concerning how many isolates should be tested.
- There are circumstances where isolates test positive to one or more of the protease tests, but the flock from which they come has no evidence of virulent disease. False positive decisions may result in the application of costly and unnecessary control and eradication programmes.
- It is unlikely also that these tests would be applicable in remote regions or developing countries.
D. nodosus may be classified into 10 or more serogroups based on agglutinin response to fimbrial antigens. Within serogroups there are one or more serotypes recognizable. These antigenic variants are found among all isolates irrespective of their virulence in vitro (Claxton et al., 1983) and are therefore of no help in characterizing outbreaks, although they may have some value in assisting tracing the origin of outbreaks. More recently, identification of genes that code for the outer membrane proteins of the organism has introduced another potentially useful epidemiological marker (Moses et al., 1995; Ghimire and Egerton, 1999).
The diagnosis of a case of footrot either clinically or with the aid of tests is not sufficient to support a decision on whether or not to commence a control or eradication programme in the flock in which it occurs. At the flock level, footrot occurs as either virulent footrot (VFR), intermediate footrot (IFR) or benign footrot (BFR), although there may be a complete spectrum of disease severity (Stewart, 1989). VFR causes the most serious lameness, weight loss and reduced wool production. In affected flocks, many animals have under-running of the sensitive laminae under the hard horn of the hoof. These severe infections persist in most affected animals irrespective of the environment. They are associated with infection by strains of D. nodosus that produce proteolytic enzymes, which are distinguishable from those associated with BFR (Stewart 1989). The presence of these so-called virulent strains is not necessarily an accurate predictor of the presence of virulent disease (Whittington, 1994). Strains of this type are isolated from episodes where only a few animals have severe disease. The recognition of these flocks led to the definition of IFR.
In flocks with IFR, many animals may have mild infections (those confined to the skin between the claws and the heel region) but these are likely to regress without treatment, as the environment becomes drier. As a working definition, IFR is an outbreak where less than 10% of animals have severe infections. Although those animals with severe infections are adversely affected, their impact over the whole flock is not severe enough to warrant expensive programmes. Recent research in Australia has indicated that IFR is not significantly affected by a change to a more favourable environment. Those animals with the most severe infections transmit a disease which, in a new flock, results again in a low proportion of severely affected animals (Abbott, 2000).
BFR is the mildest form of footrot. The infections are predominately confined to the IDS, although a few animals in the flock may have severe lesions. By convention this is about 1% of exposed animals. Again it is characteristic of BFR that most affected animals heal when the environment dries. The disease may cause lameness but this is temporary and unlikely to cause production losses. There are two important features of the strains of D nodosus associated with BFR. Their relatively heat labile proteolytic enzymes are an accurate predictor of the type of footrot in the flock so they are useful in confirming the nature of the disease present (The Woolmark Company, 1996). However, mixed infections with benign and virulent organisms are common and caution should be used in classifying outbreaks on the basis of in vitro tests on a few isolates only. These mild strains are frequently present in the feet of infected cattle. Cattle are therefore a reservoir of infection for sheep (Egerton, 1989). The occurrence of benign strains of D. nodosus in cattle makes it unlikely that BFR can be eradicated from farms that graze both sheep and cattle. There is little or no evidence that strains of D. nodosus from VFR or IFR are able to infect cattle. Because footrot control and eradication programmes are expensive and their cost is usually carried by owners, it is essential that the form of footrot in a flock is diagnozed accurately.
In principle, a decision to undertake either eradication or control should be based on an analysis of the economic impact of the disease on the flock, and the risk it represents for nearby flocks. The likely cost of the programme and its chance of success should also be considered. The interaction of the major components in deciding whether or not to intervene is illustrated in figure 1.
Flock Diagnosis: A method for identifying clinical form of footrot in flocks.
The following discussion refers to sheep, and the lesion scoring system described is applicable to that species only. The majority of goats infected with strains virulent for sheep may have infections confined to the interdigital skin.
The method of lesion scoring aims to examine sufficient sheep to be confident that a representative sample of the disease has been observed. As each sheep is examined, a score is allocated to each of the feet. A simple and repeatable scoring system (Egerton and Roberts, 1971) is one with a scale from 0 to 4 (see pictures). A score of 0 is given to normal feet. Score 1 infections are non-specific and may be the consequence of exposure to wet pastures and environmental bacteria. Score 2 are those infections in which there is inflammation, exudation and necrosis of the IDS only. Score 3 involves under-running of the soft horn of the heel and sole. An infection of score 4 is defined as one in which the necrotic process extends under the hard horn either on the axial surface of the claw, the toe or the abaxial wall. When the sample of sheep has been examined, the percentage of sheep with score 4 infections in the total of those with scores of 2 or greater (affected animals) will help in making a diagnosis.
Thus in VFR this percentage is 10% or greater while in IFR the percentage of severe cases is between 1 and 10%. In BFR outbreaks, 1% or less of affected animals will have severe (score 4) infections. When a high percentage of sheep examined have score 4 infections in at least one foot VFR is easily diagnozed. As the proportion of sheep with score 4 infections decreases it is necessary to examine more sheep to be confident that the estimate obtained from the sample is accurate. This approach to flock diagnosis presupposes that the disease present has expressed itself adequately. If there is doubt about inhibitory effects of environment or prior treatment on the expression of the disease, it may be necessary to re-examine the flock after an interval of two or more weeks. The prevalence of score 4 infections, which represents the threshold between VFR and IFR, is a matter of debate (Walker, 1997; Allworth and Egerton, 1999; Abbott, 2000). Clearly the objective of diagnosis should always be to identify disease that is economically important and not to waste resources on disease that has a transient and trivial impact on sheep flocks.
This approach to flock diagnosis may be supported by one or more of the laboratory tests described above (Walker, 1997).
List of Symptoms/SignsTop of page
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Sign|
|General Signs / Fever, pyrexia, hyperthermia||Sign|
|General Signs / Forefoot swelling, mass front foot, feet||Sign|
|General Signs / Forefoot swelling, mass front foot, feet||Sign|
|General Signs / Forefoot swelling, mass front foot, feet||Sign|
|General Signs / Forelimb lameness, stiffness, limping fore leg||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|General Signs / Forelimb swelling, mass in fore leg joint and / or non-joint area||Sign|
|General Signs / Generalized lameness or stiffness, limping||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
|General Signs / Hindfoot swelling, mass rear foot, feet||Sign|
|General Signs / Hindfoot swelling, mass rear foot, feet||Sign|
|General Signs / Hindfoot swelling, mass rear foot, feet||Sign|
|General Signs / Hindlimb lameness, stiffness, limping hind leg||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|General Signs / Hindlimb swelling, mass in hind leg joint and / or non-joint area||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|General Signs / Reluctant to move, refusal to move||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Weight loss||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Sign|
|Pain / Discomfort Signs / Forefoot pain, front foot||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Pain / Discomfort Signs / Forelimb pain, front leg||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Pain / Discomfort Signs / Hindfoot pain, rear foot||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Pain / Discomfort Signs / Hindlimb pain, hind leg||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Pain / Discomfort Signs / Skin pain||Sign|
|Pain / Discomfort Signs / Skin pain||Sign|
|Reproductive Signs / Agalactia, decreased, absent milk production||Sign|
|Skin / Integumentary Signs / Defective growth of nail, claw, hoof||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
|Skin / Integumentary Signs / Foul odor skin, smell||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Skin / Integumentary Signs / Heat, nail, claw, hoof, hot, warm||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Skin / Integumentary Signs / Hyperkeratosis, thick skin||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Sign|
|Skin / Integumentary Signs / Moist skin, hair or feathers||Sign|
|Skin / Integumentary Signs / Nail, claw, hoof sloughing, separation||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
|Skin / Integumentary Signs / Nail, claw, hoof, abscess, ulcer, under-run||Sign|
|Skin / Integumentary Signs / Nail, claw, hoof, abscess, ulcer, under-run||Sign|
|Skin / Integumentary Signs / Nail, claw, hoof, abscess, ulcer, under-run||Sign|
|Skin / Integumentary Signs / Overgrown nail, claw, hoof||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
|Skin / Integumentary Signs / Skin erythema, inflammation, redness||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
|Skin / Integumentary Signs / Skin fistula, sinus||Sign|
|Skin / Integumentary Signs / Skin ulcer, erosion, excoriation||Cattle & Buffaloes:All Stages,Other:All Stages,Sheep & Goats:All Stages||Diagnosis|
Disease CourseTop of page
The pathogenesis of footrot has been studied in sheep and it is likely that similar processes occur in other hosts.
New cases of footrot develop when animals with predisposed interdigital skin come into contact with D. nodosus. In experimental infections, there is initial multiplication and invasion of the epidermis by environmental bacteria including F. necrophorum. After about four days it is possible to identify the characteristic cells of D. nodosus in tissue sections. Theseorganisms, if virulent, advance from the epidermis of the interdigital skin to the sensitive laminae underlying the soft horn of the heel region of the hoof. This takes approximately 10 days and is accompanied by moderate to severe inflammation of the affected part of the interdigital skin. As the mixed infection advances through the germinal layer, it separates the horn of the hoof from its underlying soft tissues (Roberts and Egerton, 1969; Hine, 1984). In the most severe cases, complete separation of the horn of the affected digit occurs within 21 days. Whether the separation is due to the direct action of proteases elaborated by D. nodosus, by the products of other bacteria or the host’s inflammatory cells has not been resolved (Stewart, 1989). However, the presence of D. nodosus isessential because its elimination by specific immunization aborts the disease (Egerton and Roberts, 1971; Egerton et al., 1996).
In less severe cases, infection may only involve the sensitive laminae of the soft horn of the heel and/or sole. In some individuals, even when the disease is virulent, infection is confined to the skin between the digits (Egerton et al., 1983).
Untreated, virulent footrot persists for many months or even years in some animals (Beveridge, 1941). In a flock affected with benign or intermediate disease, many animals appear to heal spontaneously with the advent of dry weather.
EpidemiologyTop of page
Environmental, agent and host factors, which affect the epidemiology of ovine footrot have been identified. In principle, these factors may also apply to D. nodosus infections in other ruminants, but with the possible exception of goats detailed information is not available. Understanding the factors that affect the epidemiology and their interactions, is a pre-requisite to development and application of rational disease management programmes in flocks and herds.
A close association between the occurrence of new cases and long term exposure to moisture has been observed, in flocks of sheep where footrot is endemic (Graham and Egerton, 1968). New cases only occurred if ambient temperatures were consistently above a mean daily temperature of 10°C. In winter rainfall regions of Australia, outbreaks of footrot occur in the spring. Areas with predominately summer rain have autumn outbreaks. It has been suggested that abnormally cold or abnormally dry weather can prevent the full expression of the virulence of a footrot outbreak (Plant, 2000). Abbott (2000) showed that changing from an alleged unfavourable environment to a favourable one had no discernible effect on the expression of ovine footrot of intermediate virulence.
D. nodosus is an obligate anaerobe and by itself is incapable of invading healthy, dry, skin (Roberts and Egerton, 1969). Histological studies of the interdigital skin of sheep chronically exposed to water and sheep faeces, showed that hydrated stratum corneum was invaded by aerobic cocci, diphtheroid organisms and by filamentous bacteria with the morphology of F. necrophorum (Egerton et al., 1969). It is likely therefore that the environmental factors above predispose to invasion by organisms normally within the environment of sheep. These, in turn, create the metabolic and physical environment necessary to facilitate the invasion and multiplication of D. nodosus. Because D. nodosus is a strict pathogen and persists in the environment for less than a week (Stewart, 1989), new infections do not occur unless there is contact between susceptible, predisposed animals and a recently contaminated environment.
The virulence of D. nodosus determines the clinical nature of outbreaks of footrot. While all these determinants have not yet been identified, the proteases elaborated by the organism are important. (Stewart, 1989). The fimbriae of D. nodosus are also essential to the infection because it can be prevented and cured with fimbrial vaccines (Egerton et al., 1987, 1996). Benign, intermediate and virulent strains have been identified (Stewart, 1989), but there is more likely to be a continuing spectrum of virulence than discrete groups of strains.
There is considerable variation in the resistance of individuals within a population. Some of this resistance has been shown to be heritable (Skerman et al., 1988; Raadsma, 2000;). In naturally occurring outbreaks, resistance may be shown by a failure to become infected, developing a less severe infection or by healing more quickly without treatment. (Egerton et al., 1983). While some breeds are considered to be particularly susceptible, some animals of all breeds are likely to succumb, given exposure to infection in a suitable environment.
Some animals which recover naturally or which respond to treatment become sub-clinical carriers. These are a source of re-infection for the flock when environmental conditions which favour a relapse, recur (Ghimire and Egerton, 1996). There is some evidence that less virulent infections are more likely to persist in this sub- clinical state (Allworth and Egerton, 1995; Egerton et al., 1996; Abbott, 2000). The failure of less invasive disease to provoke a measurable, fimbrial agglutinin response may account for this (Whittington, 1996).
Cattle (Toussaint and Cornelisse, 1971; Egerton and Laing, 1978; Hirigoyen and Bermudez, 1991), goats (Claxton and O'Grady, 1986) and deer(Skerman, 1983) are also infected by D. nodosus. The strains of D. nodosus isolated from cattle are benign for sheep. By contrast, some isolates from goats are virulent for sheep, others are benign (Egerton, 1989; Ghimire and Egerton, 1999). Strains that are virulent for sheep do not seem to infect cattle, but they can cause serious disease in goats and vice versa (Ghimire and Egerton, 1999). Insufficient isolations have been made from deer to allow any decision on their role as reservoirs of isolates virulent for sheep, cattle or goats. There is no evidence that animals other than ruminants or inanimate objects transfer the organism between flocks or herds.
Impact: EconomicTop of page
In sheep, animals affected with footrot are lighter and produce less wool of a lower quality (Marshall et al., 1991). Abbott (2000) demonstrated the relationship between the severity of footrot in individual sheep within a flock, and the depression of their wool production and body weight. Economically, the impact of uncontrolled virulent footrot, is much greater than that of less severe forms of the disease. It has been estimated that overall, footrot can cost between US $5-10 annually for each sheep in an affected flock (Stewart, 1989). In Brazil, the annual loss in wool production has been estimated to be US $1 million (Ribeiro, 2000).
There are some effects of footrot, which are difficult to measure. Badly affected animals are obviously in pain and their welfare is impaired. Poorly designed and badly executed control programmes result in avoidable expense. In those husbandry systems that include annual migrations, affected sheep and goats are less mobile and more susceptible to predators (Ghimire and Egerton, 1996).
Serous exudate from footrot is attractive to a number of flies. In Australia, Lucilia cuprina commonly oviposits in affected feet (Watts et al., 1976). Larvae then transfer to the fleece of recumbent sheep and result in fly strike and further wool loss (Stewart, 1989; Marshall et al., 1991). In South America, footrot attracts the new-world screwworm fly, Cochliomya hominovorax. Penetration of the deeper tissues by their larvae results in severe cases of foot abscess (Egerton and Raadsma, 2000). The impact of D. nodosus infection and its sequelae has not been measured objectively in cattle or goats.
Zoonoses and Food SafetyTop of page
D. nodosus is not a human pathogen. Of the other bacteria known to occur in footrot, F. necrophorum is a potential source of infection for people handling infected sheep. Hygienic precautions and disinfection of abrasions and wounds should be part of work practice. Compliance with withdrawal times will ensure that drug residues are not a hazard in the tissues of animals treated with antibiotics.
Disease TreatmentTop of page
Depending on the resources available, some detailed attention may be given to affected animals at the conclusion of intensive footbathing or after a vaccination programme.
Traditionally, ovine footrot has been treated by foot trimming before topical application of antibacterials. However, some studies suggest that foot triming can in fact be counterproductive, delaying healing (Green and Kaler, 2011; Kaler et al., 2010).
If permitted under food hygiene regulations, parenteral antibiotic treatment has been shown to be effective (Venning et al., 1990; Ware et al., 1994; Egerton, 2000; Kaler et al., 2010; Wassink et al., 2010; Green et al., 2012; Strobel et. al, 2014).
It is essential to the success of parenteral treatment that animals be kept in a dry environment for the 24 hours following injection (Jordan et al., 1996).
A randomized clinical trial conducted in the UK (Kaler et al., 2010) reported that sheep receiving systemic antibacterials recovered faster from lameness than positive controls, whereas sheep foot trimmed recovered more slowly than positive controls. The cure rate in ewes treated with long acting systemic oxytetracycline in combination with topical oxytetracycline was estimated to be 72% within 5 days, compared with a cure rate of 11% in ewes treated with foot trimming in combination with topical oxytetracycline.
A study of the opinions of veterinarians on the efficacy of treatments for ovine footrot found that a diverse spectrum of clinical beliefs exists with respect to the efficacy of systemic and topical oxytetracycline versus foot trimming and topical oxytetracycline (Higgins et al., 2013).
Table: Recommended single doses for parenteral antibiotic treatment of virulent footrot (Egerton, 2000. Reproduced with permission of Blackwell Science Ltd.).
|Antibiotic||Dose i/m||Withholding period (days)|
|Procaine penicillin/Dihydrostreptomycin sulfate||70 000 U/kg+ 70 mg/kg||28|
|Oxytetracycline LA 200 mg/ml||1 ml/10 kg||42|
|Lincomycin HCLMonohydrate/spectinomycinSO4 tetrahydrate(Lincomycin base 50mg/mlSpectinomycin base 100mg/ml)||1 ml/10 kg||28 days|
|Erythromycin base 200 mg/ml||0.2 ml/10kg||3|
Intensive and frequent footbathing during the transmission phase, with or without vaccination, can reduce the prevalence of VFR to acceptable levels. Combined with treatment or culling of residual cases after transmission has ceased it should reduce the economic impact of footrot to an acceptable level. The process needs to be repeated in each successive year.
Prevention and ControlTop of page
After diagnosis of VFR, control rather than eradication, may be preferable. This would be the case in a flock that regularly introduces sheep from flocks of unknown footrot status. It may also be desirable where the flock is surrounded by other affected flocks, and where straying sheep cannot be excluded with confidence. It is obvious also, that where sheep are traded in public markets, which do not exclude footrot, there is a continuing potential for introduction and transfer of the disease. If the prevalence of disease is high, it is better to attempt control than eradication in the first instance.
Principles of control: Control programmes should give the maximum benefit from the least possible outlay in time and money. For this reason they should be directed at the flock as a unit rather than at individual sheep. There are two principal objectives of a control programme. These are to limit the spread of the disease and to reduce the impact of the disease in those animals that do become infected. Such a control programme should be based on an understanding of the seasonal behaviour of footrot in the area in which the flock is located. There are periods of the annual cycle in which effort should be intensified, while at other times less input will be required. For example, if it is known when transmission is most likely to occur, preventive measures should be applied intensively just before and during this period.
Preventive measures: Frequent footbathing in solutions of formalin, zinc sulphate or copper salts have been shown to limit the spread of footrot in flocks ( Stewart, 1989; Reed and Alley,1996). The key to the success of a footbathing programme is its frequency. For optimum effect the whole of the flock at risk should be walked through the footbath solution at least once weekly during times conducive to transmission. Topical solutions used in this way prevent the invasion of bacteria beyond the interdigital skin and thus limit the severity of disease in many animals. For efficiency in treating the whole flock during transmission, footbathing should be done without preparation of the feet of individual sheep. Those animals with severe infections will benefit from the footbathing, but will not be cured. Time and effort should not be wasted attempting to cure animals at times when re-infection is likely to occur. Each of the chemicals listed is equally effective for control, but zinc sulphate and copper salts are less painful for the sheep and more pleasant for the operators.
Vaccination: Vaccines that are formulated to contain the major known serogroups of D. nodosus can be successful in the control of footrot (Stewart, 1989; Liardet and Hamilton 1989; Liardet et al. 1989). They have two effects; they prevent infection in a proportion of the flock and they also accelerate cure in those animals, which are already affected. Ideally the first course of vaccination should be complete before transmission is likely to occur. However, where prevalence is high it may be desirable to vaccinate to derive early benefit from their therapeutic effect. Multivalent vaccines are limited in their usefulness by the short period of immunity, which follows their use. Specific vaccination is much more effective if the identity of antigenic types in the flock is known or can be determined (Egerton et al., 1996; Urbaneck et al., 1998; Dhungyel et al., 2008; Dhungyel et al., 2013). Again, increased value can be obtained from the vaccine if it is applied prior to the known transmission periods. Annual revaccination needs to be timed according to what is known of the seasonal cycle of the disease.
Selective breeding: It has been proposed that long-term control may be feasible through selective breeding (Raadsma and Dhungyel, 2013). Genetic variation among breeds, strains with breeds and genetic differences within flocks all provide avenues to reduce susceptibility and therefore impact of the disease. The heritability of resistance is in the range of 15-25% and provides a means to identify animals with superior breeding values based on clinical examination of affected individuals or progeny from candidates under selection. The use of DNA markers based on whole genome selection using high density markers is likely to be successful to identify resistant animals in absence of disease, but will be breed and flock specific. Selective breeding for increased resistance is unlikely to directly impact negatively on genetic change in other production or disease traits, but will reduce genetic gain in such traits by the inclusion of footrot in a multi-trait breeding objective. Selective breeding for resistance is unlikely to be of value in case of benign footrot or when eradication is sought.
Eradication of footrot
Principles of eradication from sheep
The transmitting agent of footrot, D. nodosus, persists only in the feet of affected animals.It does not persist in the environment for more than seven days. Eradication of footrot requires the elimination, within a flock, of all cases of infection with D. nodosus. Normally only VFR and perhaps IFR are targets for eradication. There are a number of prerequisites for successful eradication of footrot from a flock. These are:
- Correct diagnosis of the flock disease
- Knowledge of transmission patterns in the flock’s environment
- Application of knowledge of seasonal patterns of disease in planning the programme for a flock
- Ability of the operator of the programme to recognise all cases of footrot
- Acceptance that while footrot is present in the flock, all cases, irrespective of severity, are cases of VFR/IFR.
- Acceptance that eradication of footrot is time consuming and costly
- Understanding that, in flocks with a high prevalence at the start of the programme, eradication may take 2 or more years to achieve, and that benign strains will persist in the flock (Egerton and Raadsma, 1993).
- Acceptance that eradication should only be attempted where the flock can be protected against re-infection from neighbours or sheep purchased from elsewhere.
Methods of eradication
- Whole flock disposal: The simplest and most effective method for the eradication of footrot is to dispose of the whole flock as soon as it is convenient after the diagnosis has been made, and to replace it two or more weeks later with animals free of the disease. This method presupposes that there is a market for the affected sheep, that disease free sheep are available and that the cost of the disposal-replacement programme is acceptable, taking into account the time and cost which is involved in alternative methods. Many of the prerequisites listed above do not apply to the disposal - replacement approach.
- Disposal of affected animals: The next simplest approach is to dispose of the infected animals in the flock. If the prevalence of infected animals is so high that their disposal would severely affect production, a season or more of control by footbathing or vaccination may be used to reduce prevalence to a level where disposal is acceptable. Success in eradication by disposal of affected animals depends on identifying every case of footrot and removing it from the flock. This can be achieved by inspecting all feet, of all sheep in the flock at least three times at intervals of approximately three weeks. These inspections should only be done at a time when transmission is unlikely to be occurring. There should not be any treatment applied to the sheep for at least three weeks before and during these inspections. Animals identified as affected should be marked and segregated in a separate flock and disposed of, preferably by sale for slaughter. The objective of eradication by disposal of affected cases is to ensure that no source of re-infection remains in the flock, when environmental conditions again favour transmission.
- Identification and treatment of affected animals: Eradication using this method is possible but the probability of success is lower than in either of the two preceding ones. The procedure for identifying affected animals i.e. repeated whole flock inspections is again used as in method 2 above. Again it is essential that there is no possibility of transmission and therefore of the presence of cases in incubation during this identification process. When cases have been identified they may be treated either topically or parenterally. This is discussed in the disease treatment text. Abbott (2000) recommends against the use of parenteral antibiotics in flocks affected with IFR, because of the increased likelihood of inducing carrier cases. Whichever method of treatment is adopted it is necessary to inspect treated animals three weeks later to identify those animals which have not responded to treatment. Even under optimally dry environmental conditions, some animals will not be cured and these should be removed from the flock.
The key to successful eradication of VFR/IFR from flocks is examination and re-examination of animals considered to be free of disease. Concentration of efforts on this component of the flock is more productive than work with affected animals. Eradication cannot be claimed until the flock has passed through at least one season known to be suitable for transmission. It is also important to recognize that after the eradication of VFR/IFR there is a high probability that BFR will persist in the flock. The methods based on identification and disposal, and identification and treatment do not usually eliminate the strains of D. nodosus associated with the benign disease. The normal sequence and the principal features of each stage of the footrot management process are summarized in the table below.
Table: Sequence and principal features of footrot management in flocks
|Phase||Objectives||Methods||Time in cycle|
|Diagnosis||Identify diseaseDetermine if VFR is present.||Clinical examinationScoring of sample of sheep||When disease is fully expressed|
|Control||Limit economic impact; reduce prevalence if goal is eradication||Frequent whole flock footbathing; vaccination||Transmission period mainly.Any time for quick effect.|
|Eradication||Eliminate all cases of footrot from flocks||a-Flock disposalb-Identify and remove all affected sheepc-identify and treat all affected sheep(b and c require repeat inspections of disease free sheep, c requires finding and removing sheep not cured)||a: anytimeb: non-transmission periodc: non-transmission period|
|Surveillance after eradication||Maintain freedom from VFR||Immediate investigation of lameness; annual whole flock inspection; ensure precautions are taken with new sheep.||Vigilance in whole cycle; annual inspection following transmission period|
Flocks free of footrot, whether following an eradication programme or not, should be subjected to a clearly defined surveillance programme. This programme includes immediate investigation of lameness, annual foot by foot inspection of all sheep and inspection of sheep before they are introduced from other flocks. If there is any evidence of footrot in any sheep being considered for purchase, or evidence of treatment for footrot the whole group should be rejected. Maintenance of freedom from VFR is highly dependent also on the status of neighbouring flocks and the integrity of fences or other barriers between farms. There should not be any requirement for any form of footrot treatment in a flock, which has successfully eradicated VFR/IFR. Surveillance and early recognition of recurrence will be inhibited by routine or even spasmodic footbathing. In the event that VFR/IFR recurs it is important to identify it early and limit it to restricted groups on the farm. An anamnestic ELISA test (Whittington and Egerton, 1994), can reveal evidence of prior infection with VFR and may be applicable to determining the status of flocks before sheep are purchased.
Eradication at regional levels
While the principles of eradication of VFR have been known and applied for half a century, the disease persists in most sheep producing countries. Even in Australia where a substantial amount of money has been invested in research and the extension of research results, there are many regions where there is a continuing high prevalence of the disease. In three states, South Australia, Western Australia and New South Wales, there has been considerable progress towards eradication. The success in New South Wales, in particular, has resulted from a number of factors that are separate from scientific understanding of the disease. The most important of these has been the enthusiastic support of the majority of sheep owners for a programme of eradication (Walker, 1997). The cost of this program has been borne principally by the sheep owners themselves. While the programme has been voluntary, it is backed by state laws that restrict owners of affected flocks from sale of diseased sheep in markets and from their using public roads to move sheep. The state’s eradication programme was given impetus by the early formation of groups of farmers who owned neighbouring properties. These groups were ideal for extension of information about the development and application of programmes for individual flocks. At the time the programme commenced, there was an extensive veterinary and para-veterinary infrastructure in the state, which supported these farmer groups in diagnosis and in the investigation of problems that arose. The programme was further supported through the establishment and implementation of a flock accreditation scheme. The stud sheep industry was a strong supporter of this and similar schemes. There was also a process whereby people selling sheep signed a formal declaration of the footrot status of those sheep and their flock of origin. These declarations were instrumental in reducing the transfer of infected animals through markets.
The programme in NSW has made substantial progress (Walker, 1996; Plant, 2000). At the beginning of the programme the flock prevalence in some districts was as high as 50%. At the outset it was estimated that there were approximately 10,000 affected flocks in the state. Now there are less than 1000. As the programme continues, it is apparent that BFR persists and that IFR is being diagnozed more frequently. This presents a challenge. In some of these flocks the severity of the disease is low but organisms which are identified as virulent in ‘in vitro’ tests have been isolated from them. There is considerable argument about the capacity of the environment to prevent full expression of disease in such flocks. Recent research however, suggests that the level of expression observed in these IFR flocks is independent of the environment (Abbott, 2000). On the other hand, there is also evidence that some of the strains of D. nodosus present in these episodes can be eradicated using conventional approaches, with one important exception regarding treatment. The use of parenteral antibiotics seems to be contra-indicated (Abbott, 2000).
In Western Australia, the programme is based on using thermostability of the proteases of D. nodosus as the single criterion for the diagnosis of VFR. IFR is not recognized as a clinical entity. As a consequence, eradication is pursued wherever a positive isolate is identified, irrespective of the severity of the disease present. Eradication of all such strains is justified on the basis of some evidence suggesting that environment does materially affect the expression of footrot of marginal severity (Depiazzi et al., 1998). In South Australia the presence of ‘stable’ strains of D. nodosus is not an accurate predictor of the type of disease present in flocks with a low prevalence of score 4 infections (McFarland and Saunders, 1996). It is true however, that the fully virulent disease has essentially been eliminated from South Australia and West Australia.
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